Simultaneous Assessment of Skeletal Muscle Energetics and Blood Flow During Dynamic Exercise by Interleaved ³¹ P ‐ MRS / ¹ H ‐ MRI

Figures

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  FIGURE 1. (A) Data acquisition protocol starting with 1H MRI scout and B0‐map for second order shimming, and fully‐relaxed 31P MRS to determine resting metabolite concentrations. The interleaved 31P MRS/1H flow MRI (shown in red) was validated against conventional (shown in blue) 31P‐MRS at rest, and cine flow acquisitions both at rest and during recovery. Recovery BF for each technique was defined as the regression intercept at the midpoint between the last interleaved acquisition and the first conventional acquisition (at 195 s of recovery shown in yellow). (B) Schematic of the interleaved 31P MRS/1H flow MRI pulse sequence alternating between 42 1H MRI flow encoded acquisitions with golden angle rotated spiral readouts and a non‐localized pulse‐acquire 31P MRS acquisition. (C) Each of the 42 flow MRI elements contained two velocity encoded phase contrast acquisitions with a TR of 19 ms, water selective spectral‐spatial excitation, and variable density spiral readouts (12 ms). The spiral trajectory was rotated by the golden angle from one flow element to the next. (D) The non‐localized 31P MRS acquisition used a BIR‐4 adiabatic excitation pulse with a 341‐ms readout acquired every 2 s.…

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  FIGURE 2. Representative 31P spectra acquired using either the conventional (A) or interleaved 31P MRS/1H MRI approach (B) in the same individual (1 average; TR = 2 s). The time course of phosphocreatine (PCr), inorganic phosphate (Pi), and adenosine triphosphate (ATP) dynamics acquired with the interleaved approach are shown in the same participant (C). As expected, PCr gradually declines during plantar flexion exercise (PFE) with a concomitant increase in Pi, while ATP is maintained throughout. The resistance in kg and power output in Watts are reported for each exercise stage.

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  FIGURE 3. Resting phosphocreatine concentration (PCr; A), inorganic phosphate concentration (Pi; B), and intracellular pH (C) were similar between those measured using the interleaved and conventional sequences in all subjects. Bland–Altman plots support this by demonstrating minimal bias in measurements of PCr (D), Pi (E), and pH (F).

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  FIGURE 4. Phase‐contrast magnitude (A and B) and velocity (C and D) images from the same participant as Figure 2 at rest prior to exercise acquired using the conventional cine approach (A and C) and the interleaved approach (B and D). The images shown are from the 16th of 40 cardiac phases where peak popliteal artery blood flow (BF) is observed. The insets show a zoomed area containing the popliteal artery. The white and black arrows identify the popliteal artery and vein respectively. Negative velocities, shown as darker image intensity, indicate flow in head‐foot direction. The popliteal artery flow profile throughout the cardiac cycle was similar between the two methods (E and F). The mean BF is listed in the top right of panels E and F.

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  FIGURE 5. In the same representative participant as Figures 2 and 4, phase‐contrast magnitude (A–D) and velocity (E–H) images acquired during recovery from exercise with the interleaved approach (A, B, E, F) and the conventional cine approach (C, D, G, H) are shown. The images shown are from the 16th of 40 cardiac phases around where peak popliteal artery blood flow (BF) is observed. Shown are the first and fourth of six interleaved flow measures acquired 30 and 120 s after exercise cessation, and the first and fourth of four conventional cine flow measures acquired 210 and 300 s after exercise. The insets show a zoomed area containing the popliteal artery. Negative velocities, shown as darker image intensity, indicate flow in head‐foot direction. The popliteal artery flow profiles throughout the cardiac cycle for each measurement (I–L) show a gradual decrease of the recovery flow back towards resting values. The mean BF results for each recovery measure are listed in the top right of panels I–L.

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  FIGURE 6. The grouped change in mean popliteal blood flow (BF) during recovery is shown in (A), with the first six measures acquired with the interleaved approach (black circles and lines) and the last four measures acquired with the conventional cine approach (red squares and lines). Data are shown as grouped mean and standard deviation. There was no significant difference in the regression fit slope between the two approaches (B).

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  FIGURE 7. Popliteal artery blood flow (BF) was assessed using both the interleaved and conventional approaches at rest (closed circles) and during recovery (open squares) from plantar flexion exercise to test the validity of the interleaved approach across a wide physiological range of BF. Shown are (A) a strong positive correlation with a slope of 0.98, (B) a lack of significant differences in paired comparisons, and (C) small bias as shown in the Bland–Altman plots. The red line in (A) represents the line of identity, and the regression equation and r 2 are stated on the figure. CI, confidence interval.

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  FIGURE 8. Phase contrast magnitude (A–E) and velocity (F–J) images acquired during plantar flexion exercise (PFE) with the interleaved approach in the same participant as in Figures 2, 4 and 5. Shown are the ninth of 15 cardiac phases demonstrating near‐peak popliteal artery blood flow (BF). Shown are the last (second) flow images from each PFE stage with the foot in the fully relaxed pedal position. The insets show a zoomed area of the popliteal artery. Negative velocities, shown as darker image intensity, indicate flow in head‐foot direction. The corresponding popliteal artery BF profiles throughout the cardiac cycle are shown below (K–O). The flow profile is almost entirely above zero during the first stage of PFE (K), and the baseline and peak of the BF profile shift significantly upwards as exercise intensity increases. The mean BF results for each PFE stage are listed in the top right of panels K–O.

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  FIGURE 9. The grouped change in popliteal artery blood flow (BF) during rest, dynamic PFE (shaded gray), and recovery is shown for each of the four PFE foot pedal positions: Partially contracted (A), fully contracted (B), partially relaxed (C), and fully relaxed (D). The flow response during the final stage of PFE was lower when the calf muscles were fully contracted to cause flexion around the ankle joint (B), as compared to when the foot was in fully relaxed position to cause dorsi flexion around the ankle joint (D), and intermediate for the two positions in between (A and C). As a result, popliteal BF overshoots from the end of PFE to the beginning of recovery once all four foot pedal positions are averaged (E). Plots represent mean ± SD. The sample size at each exercise stage is noted in panel E but are consistent across all other panels (A–D). The decrease in sample size with greater exercise intensity reflects the drop out in participants due to reaching fatigue. The average BF in the final PFE stage is plotted before the recovery curves.